Inoculation with bacterial endophytes and the fungal root endophyte, Piriformospora indica improves plant growth and reduces foliar infection by Phytophthora capsici in black pepper

Inoculation with bacterial endophytes and the fungal root endophyte, Piriformospora indica improves plant growth and reduces foliar infection by Phytophthora capsici in black pepper


  • Teenu Paul College of Agriculture, Kerala Agricultural University, Thiruvananthapuram 695 522, Kerala, India
  • N.S. Nysanth College of Agriculture, Kerala Agricultural University, Thiruvananthapuram 695 522, Kerala, India
  • M.S. Yashaswini College of Agriculture, Kerala Agricultural University, Thiruvananthapuram 695 522, Kerala, India
  • K. N. Anith kerala agricultural university college of agriculture, vellayani


Foot rot disease caused by the oomycete fungus Phytophthora capsici is one of the major problems faced by black pepper growers. Two bacterial endophytes, Bacillus velezensis PCSE10 and Rhizobium radiobacter PCRE 10 isolated from the wild relative of black pepper, Piper colubrinum, and the root endophytic fungus, Piriformospora indica and their combined effect were evaluated for plant growth promotion and suppression of foliar infection caused by P. capsici in bush pepper plants (var. Panniyur 1). B. velezensis PCSE10 exhibited in vitro antagonism against P. capsici. In a detached leaf assay, R. radiobacter PCRE10 significantly reduced the lesion size. R. radiobacter PCRE10 was found to be compatible with P. indica in dual culture plate assay. Suppression of foliar infection of P. capsici in plants treated with the individual endophytes and their combination was assessed by challenge inoculation with the pathogen on the foliage. Plants treated with combination of P. indica and R. radiobacter PCRE10 recorded lowest lesion size (0.43 cm), which recorded 10.41 per cent disease suppression over the pathogen control with the lowest disease index of 0.2. Disease suppression on inoculation with P. indica was the least compared to all other treatments. Combined application of P. indica and R. radiobacter PCRE10 as well as single inoculation of P. indica showed discernible improvement in growth parameters of bush pepper (var. Panniyur 1). Plants treated with single inoculation of P. indica showed the highest fungal root colonization of 35.50% followed by the combination of P. indica and B. velezensis (31.10%), as well as P. indica and R. radiobacter PCRE10 (19.35%).

Author Biography

K. N. Anith, kerala agricultural university college of agriculture, vellayani

profesor of microbiologydepartment of agricultural microbiology


Ali, B. and Hasnain, S. 2007. Potential of bacterial indoleacetic acid to induce adventitious shoots in plant tissue culture. Lett. Appl. Microbiol. 45(2): 128-133.

Anith, K.N., Aswini, S., Varkey, S., Radhakrishnan, N.V., and Nair, D.S. 2018. Root colonization by the endophytic fungus Piriformospora indica improves growth, yield and piperine content in black pepper (Pipernigurm L.). Biocatalysis Agric. Biotechnol. 14: 215-220.

Anith, K.N., Faseela, K.M., Archana, P.A., and Prathapan, K.D. 2011. Compatability of Piriformospora indica and Trichodermaharzianum as dual inoculants in black pepper (Piper nigrum L.). Symbiosis 55: 11-17.

Anith, K.N., Radhakrishnan, N.V., and Manomohandas, T.P. 2003. Screening of antagonistic bacteria for biological control of nursery wilt of black pepper (Piper nigrum L.). Microbiol. Res. 158: 91-97.

Aravind, R., Kumar, A., Eapen, S.J. and Ramana, K.V. 2009. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation, identification and evaluation against Phytophthora capsici. Lett. Appl. Microbiol. 48: 58-64.

Aravind, R., Kumar, A. and Eapen, S.J. 2012. Pre-plant bacterization: A strategy for delivery of beneficial endophytic bacteria and production of disease-free plantlets of black pepper (Piper nigrum L.). Arch. Phytopathol. Plant Prot. 45: 1115-1126.

Ashar, V.S. 2019. Management of brown spot disease of rice using fungal root endophyte Piriformospora indica and new generation fungicides. M.Sc. (Ag) thesis, Kerala Agricultural University, Thrissur, 130p.

Athira, S. 2018. Management of bacterial wilt disease of tomato by the root endophytic fungus Piriformospora indica, rhizobacteria and bacterial endophytes. M.Sc. (Ag) thesis, Kerala Agricultural University, Thrissur, 145p.

Bailey, B.A., Bae, H., Strem, M.D., Crozier, J., Thomas, S.E., Samuels, G.J., Vinyard, B.T., and Holmes, K.A. 2008. Antibiosis, mycoparasitism, and colonization success for endophytic Trichoderma isolates with biological control potential in Theobroma cacao. Biol. Control 46: 24-35.

Baker, R. 1968. Mechanisms of biological control of soil borne plant pathogens. Annu. Rev. Phytopathol.6: 263-294.

Bianco, C., Imperlini, E., Calogero, R., Senatore, B., Pucci, P., and Defez, R. 2006. Indole-3-acetic acid regulates the central metabolic pathways in Escherichia coli. Microbiol. 152: 2421-2431.

Bressan, W. and Borges, M.T. 2004. Delivery methods for introducing endophytic bacteria into maize. Bio Control 49(3): 315-322.

Chakraborty, U. and Purkayastha, R.P. 1984. Role of rhizobitoxine in protecting soybean roots from Macrophomina phaseolina. Can. J. Microbiol. 30: 285-289.

Chandran, K. 2019. Management of Blackeye cowpea mosaic virus using natural products from botanicals and the fungal root endophyte Piriformospora indica. M.Sc. (Ag) thesis, Kerala Agricultural University, Thrissur, 108p.

Dicto, J. and Manjula, S. 2005. Identification of elicitor-induced PR5 gene homologue in Piper colubrinum Link by suppression subtractive hybridization. Curr. Sci. 88: 624-627.

Dennis, C. and Webster, J. 1971. Antagonistic properties of species groups of Trichoderma III hyphal interaction. Trans. Brit. Mycol. Soc. 57: 363-369.

Deshmukh, S., Huckelhoven, R., Schafer, P., Imani, J., Sharma, M., Weiss, M., Waller, F., and Kogel, K.H. 2006. The root endophytic fungus Piriformospora indica requires host cell death for proliferation during mutualistic symbiosis with barley. Proc. Natl. Acad. Sci. USA. 103: 18450-18457.

Ehteshamul‐Haque, S. and Ghaffar, A. 1993. Use of rhizobia in the control of root rot diseases of sunflower, okra, soybean and mung bean. J. Phytopathol. 138(2): 157-163.

Fakhro, A., Andrade-Linares, D.R., Von Bargen, S., Bandte, M., Buttner, C., Grosch, R., Schwarz, D., and Franken, P. 2010. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza 20: 191-200.

Ghorbanpour, M., Omidvari, M., Abbaszadeh-Dahaji, P., Omidvar, R., and Kariman, K. 2018. Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biol. Control 117; 147-167.

Gordan, S.A. and Weber, R.P. 1951. Calorimetric estimation of indole acetic acid. Plant Physiol. 26: 192-195.

Govindarajan, M., Kwon, S.W., and Weon, H.Y. 2007. Isolation, molecular characterization and growth-promoting activities of endophytic sugarcane diazotroph Klebsiella sp. GR9. World J. Microbiol. Biotechnol. 23: 997-1006.

Govindasamy, V., Raina, S.K., George, P., Kumar, M., Rane, J., Minhas, P.S. and Vittal, K.P.R. 2017. Functional and phylogenetic diversity of cultivable rhizobacterial endophytes of sorghum [Sorghum bicolor (L.) Moench]. Antonie van Leeuwenhoek 110: 925-943.

Guerinot, M. L., Meidl, E. J., and Plessner, O. 1990. Citrate as a siderophore in Bradyrhizobium japonicum. J. Bacteriol. 172(6): 3298-3303.

Hilbert, M., Voll, L. M., Ding, Y., Hofmann, J., Sharma, M., and Zuccaro, A. 2012. Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytologist 196: 520-534.

Islam, S., Akanda, A.M., Prova, A., Islam, M.T., and Hossain, M.M. 2016. Isolation and Identification of plant growth promoting rhizobacteria from cucumber rhizosphere and their effect on plant growth promotion and disease suppression. Front Microbiol. 6: 1360.

Jasim, B., Jimtha, C.J., Jyothis, M., and Radhakrishnan, E.K. 2013. Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul. 71: 1-11.

Johnson, J.M., Alex, T., and Oelmuller, R. 2014. Piriformospora indica: The versatile and multifunctional root endophytic fungus for enhanced yield and tolerance to biotic and abiotic stress in crop plants. J. Trop. Agric. 52: 103-122.

Kollakkodan, N. 2017. Biocontrol potential of plant associated bacteria from Piper spp. Against Phytophthora capsici infecting black pepper. M.Sc. (Ag) thesis, Kerala Agricultural University, Thrissur, 131p.

Kollakkodan, N., Anith, K.N. and Radhakrishnan, N.V. 2017. Diversity of endophytic bacteria from Piper spp. with antagonistic property against Phytophthora capsici causing foot rot. J. Trop. Agric. 55: 63-70.

Lakshmana, M., Hanumanthappa, M., and Sunil, C. 2016. Effect of propagation method on successful growth performance of pepper plants. In: Proceedings - National Seminar on Planting Material Production in Spices, (eds.) Malhothra, S.K., Kandiannan, K., Raj, K.M., Neema, V.P., Prasath, D., Srinivasan, V., Cheriyan, H., and Femina, Directorate of Arecanut and Spices Development, Kohzikode, Kerala, India: 124-129.

Lakshmipriya, P., Nath, V.S., Veena, S.S., Anith, K.N., Sreekumar, J., and Jeeva, M.L. 2017. Piriformospora indica, a cultivable endophyte for growth promotion and disease management in taro (Colocasia esculenta L.). J. Root Crops 42(2): 107-114.

Lemessa, F. and Zeller, W., 2007. Screening rhizobacteria for biological control of Ralstonia solanacearum in Ethiopia. Biol. Control 42(3): 336-344.

Li, W., Roberts, D.P., Derby, P.D., Meyer, S.L.F., Lohrke, S., Lumsden, R.D., and Hebbar, K.P. 2002. Broad spectrum anti-biotic activity and disease suppression by the potential biocontrol agent Burkholderia ambifaria BC-F. Crop Prot. 21:129-135.

Melnick, R.L., Zidack, N.K., Bailey, B.A., Maximova, S.N., Guiltinan, M., and Backman, P.A. 2008. Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biol. Control 46: 46- 56.

Mol, R.K.A., Harsha, K.N., Saju, K.A., and Kumar, P.K. 2017. Evaluation of potting mixtures and humidity conditions for rooting and establishment of plagiotropic branches of black pepper (Piper nigrum L.). Ann. Plant Sci. 6: 1622- 1624.

Molitor, A., Zajic, D., Voll, L.M., Pons-Kühnemann, J., Samans, B., Kogel, K.H., and Waller, F. 2011. Barley leaf transcriptome and metabolite analysis reveals new aspects of compatibility and Piriformospora indica- mediated systemic induced resistance to powdery mildew. Mol. Plant Microbe Interact. 24: 1427-1439.

Morath, S.U., Hung, R., and Bennett, J.W. 2012. Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol. Rev. 26: 73- 83.

Nandana, M.S. 2019.Growth promotion in chilli (Capsicum annuum L.) on inoculation with pseudomonas fluorescens and piriformospora indica. M.Sc. (Ag) thesis, Kerala Agricultural University, Thrissur, 130p.

Narayan, O.P., Verma, N., Singh, A.K., Oelmüller, R., Kumar, M., Prasad, D., Kapoor, R., Dua, M., and Johri, A.K., 2017. Antioxidant enzymes in chickpea colonised by Piriformospora indica participatein defense against the pathogen Botrytis cinerea. Sci. Rep. 7, 13553. Available: https://[ 12 June 2020]

Narisawa, K, Usuki, F., and Hashiba, T. 2004. Control of verticillium yellows in Chinese cabbage by the dark septate endophytic fungus LtVB3. Phytopathol. 94: 412–418.

Oelmuller, R., Sherameti, I., Tripathi, S., and Varma, A. 2009. Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49: 1–17.

Pedrotti, L., Mueller, M.J., and Waller, F. 2013. Piriformospora indica root colonisation triggers local and systemic root responses and inhibits secondary colonisation of distal roots. PLoS One 8 (7) e69352.Available: https://doi:10.1371/journal.pone.0069352.g002. [21 June 2020].

Prakash, K.M., Manoj, P.S., Radhakrishnan, P. Bush pepper-A profitable venture by an innovative farmer. In: Proceedings - National Seminar on Planting Material Production in Spices, (eds. Malhothra, S.K., Kandiannan, K., Raj, K.M., Neema, V.P., Prasath, D., Srinivasan, V., Cheriyan, H., and Femina), Directorate of Arecanut and Spices Development, Kohzikode, Kerala, India (2016): 233-234.

Prasad, M.P. and Dagar, S. 2014. Identification and characterization of Endophytic bacteria from fruits like Avacado and Black grapes. Int. J. Curr. Microbiol. Appl. Sci.3(8): 937-947.

Ravindran, P.N. and Remashree, A.B. 1998. Anatomy of Piper colubrinum Link. J. Spices Aromat. Crops.7(2): 111-123.

Sarma, Y.R., Anandaraj, M., and Rajan, P.P. 1994. Phytophthora, A threat to black pepper: Present status and future strategies of disease management. Spice India 7: 10-13.

Schroth, M.N. and Hancock, J.G. 1981. Selected topics in biological control. Annu. Rev. Microbiol. 35: 453-476.

Schulz, B. and Boyle, C. 2006. What are endophytes? In: Scultz, B., Boyle, C., and Sieber, T. (eds), Microbial Root Endophytes. Springer, Berlin, Heidelberg. pp 1-10.

Serfling, A., Wirsel, S.G.R., Lind, V. and Deising, H.B. 2007. Performance of the biocontrol fungus Piriformospora indica on wheat under greenhouse and field conditions. Phytopathol. 97: 523-531.

Shahollari, B., Vadassery, J., Varma, A. and Oelmuller, R. 2007. A leucine-rich repeat protein is required for growth promotion and enhanced seed production mediated by the endophytic fungus Piriformospora indica in Arabidopsis thaliana. Plant J. 50: 1-13.

Shahollari, B., Varma, A. and Oelmuller, R. 2005. Expression of a receptor kinase in Arabidopsis roots is stimulated by the basidiomycete Piriformospora indica and the protein accumulates in Triton X100 insoluble plasma membrane microdomains. J. Plant Physiol. 162: 945-958.

Sharma, M., Schmid, M., Rothballer, M., Hause, G., Zuccaro, A., Imani, A.J., Kämpfer, A., Domann, E., Schäfer, P., Hartmann, A., and Kogel, K.H. 2008. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell. Microbiol. 10(11); 2235-2246.

Sherameti, I., Tripathi, S., Varma, A., and Oelmuller, R. 2008. The root colonizing endophyte Pirifomospora indica confers drought tolerance in Arabidopsis by stimulating the expression of drought stress-related genes in leaves. Mol. Plant Microbe Interact. 21: 799-807.

Sreeja, K., Anandaraj, M., and Bhai, R.S. 2016. In vitro evaluation of fungal endophytes of black pepper against Phytophthora capsici and Radopholus similis. J. Spices Aromat. Crops. 25 (2): 113-122.

Strzelczyk, E. and Pokojska, B.A. 1984. Production of auxins and gibberellin like substances by mycorrhizal fungi, bacteria and actinomycetes isolated from soil and myco-rhizosphere of pine (Pinus silvestris L.). Plant Soil 81: 185-194.

Sturz, A.V., Christie, B.R. and Nowak, J. 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit. Rev. Plant Sci. 19: 1-30.

Tu, J.C. 1978. Protection of soybean from severe Phytophthora root rot by Rhizobium. Physiol. Plant Pathol. 12(2): 233-236.

Varkey, S., Anith, K.N., Narayana, R., and Aswini, S., 2018. A consortium of rhizobacteria and fungal endophyte suppress the root-knot nematode parasite in tomato. Rhizosphere 5: 38-42.

Varma, A., Verma, S., Sudha, S., Sahay, N., Butehorn, B., and Franken, P. 1999. Piriformospora indica, a cultivable plant growth promoting root endophyte. Appl. Environ. Microbiol. 65: 2741-2744.

Verma, S., Varma, A., Rexer, K.H., Hassel, A., Kost, G., Sarbhoy, A., Bisen, P., Butehorn, B. and Franken, P. 1998. Piriformospora indica, gen. et sp. nov., a new root-colonizing fungus. Mycologia 90: 898-905.

Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., Fischer, M., Heier, T., Huckelhoven, R., Neumann, C., von Wettstein, D., Franken, P., and Kogel, K.H. 2005. The endophytic fungus Piriformospora indica reprograms barley to salt stress tolerance, disease resistance, and higher yield. Proc. Natl. Acad. Sci. USA, 102: 13386-13391.

Wang, H., Zhneg, J., Ren, X., Yu, T., Varma, A., Lou, B., and Zheng, X. 2015. Effects of Piriformospora indica on the growth, fruit quality and interaction with Tomato yellow leaf curl virus in tomato cultivars susceptible and resistance to TYCLV. Plant Growth Reg. 76: 303-313.

Weiss, M., Selosse, M.A., Rexer, K.H., Urban, A. and Oberwinkler, F. 2004. Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol. Res. 108: 1003-1010.

Wong, P.T.W. and Baker, R. 1984. Suppression of wheat takeall and ophiobolus patch by fluorescent pseudomonads from a Fusarium suppressive soil. Soil Biol. Biochem. 16: 347-403.

Yadav, V., Kumar, M., Deep, D.K., Kumar, H., Sharma, R., Tripathy, T., Tuteja, N., Saxena, A.K. and Johri, A.K. 2010. A Phosphate transporter from a root endophytic fungus Piriformospora indica plays a role in the phosphate transfer to the plants. J. Biol. Chem. 285: 26532-26544.

Yingwu, S., Kai, L., and Li, C. 2009. Isolation, quantity distribution and characterization of endophytic microorganisms within sugar beet. Afr, J. Biotechnol. 8(5): 835–840.

Zarea, M.J., Hajinia, S., Karimi, N., Goltapeh, E.M., Rejali, F., and Varma, A. 2012. Effect of Piriformospora indica and Azospirillum strains from saline or non-saline soil on mitigation of the effects of NaCl. Soil Biol. Biochem. 45: 139-146.




How to Cite

Paul, T., Nysanth, N., Yashaswini, M., & Anith, K. N. (2022). Inoculation with bacterial endophytes and the fungal root endophyte, Piriformospora indica improves plant growth and reduces foliar infection by Phytophthora capsici in black pepper. Journal of Tropical Agriculture, 59(2). Retrieved from



Short communications